O antigen biogenesis sensitises Escherichia coli K-12 to bile salts, providing a plausible explanation for its evolutionary loss

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dc.contributor.authorQin, J.
dc.contributor.authorHong, Y.
dc.contributor.authorMorona, R.
dc.contributor.authorTotsika, M.
dc.contributor.editorHughes, D.
dc.date.issued2023
dc.descriptionPublished: October 4, 2023
dc.description.abstractEscherichia coli K-12 is a model organism for bacteriology and has served as a workhorse for molecular biology and biochemistry for over a century since its first isolation in 1922. However, Escherichia coli K-12 strains are phenotypically devoid of an O antigen (OAg) since early reports in the scientific literature. Recent studies have reported the presence of independent mutations that abolish OAg repeating-unit (RU) biogenesis in E. coli K-12 strains from the same original source, suggesting unknown evolutionary forces have selected for inactivation of OAg biogenesis during the early propagation of K-12. Here, we show for the first time that restoration of OAg in E. coli K-12 strain MG1655 synergistically sensitises bacteria to vancomycin with bile salts (VBS). Suppressor mutants surviving lethal doses of VBS primarily contained disruptions in OAg biogenesis. We present data supporting a model where the transient presence and accumulation of lipid-linked OAg intermediates in the periplasmic leaflet of the inner membrane interfere with peptidoglycan sacculus biosynthesis, causing growth defects that are synergistically enhanced by bile salts. Lastly, we demonstrate that continuous bile salt exposure of OAg-producing MG1655 in the laboratory, can recreate a scenario where OAg disruption is selected for as an evolutionary fitness benefit. Our work thus provides a plausible explanation for the long-held mystery of the selective pressure that may have led to the loss of OAg biogenesis in E. coli K-12; this opens new avenues for exploring long-standing questions on the intricate network coordinating the synthesis of different cell envelope components in Gram-negative bacteria.
dc.description.statementofresponsibilityJilong Qin, Yaoqin Hong, Renato Morona, Makrina Totsika
dc.identifier.citationPLoS Genetics, 2023; 19(10):e1010996-1-e1010996-21
dc.identifier.doi10.1371/journal.pgen.1010996
dc.identifier.issn1553-7390
dc.identifier.issn1553-7404
dc.identifier.orcidMorona, R. [0000-0001-7009-7440]
dc.identifier.urihttps://hdl.handle.net/2440/139734
dc.language.isoen
dc.publisherPublic Library of Science (PLoS)
dc.relation.granthttp://purl.org/au-research/grants/arc/DP210101317
dc.rights© 2023 Qin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
dc.source.urihttps://doi.org/10.1371/journal.pgen.1010996
dc.subjectEscherichia coli
dc.subjectEscherichia coli K12
dc.subjectBile Acids and Salts
dc.subjectO Antigens
dc.subjectEscherichia coli Proteins
dc.titleO antigen biogenesis sensitises Escherichia coli K-12 to bile salts, providing a plausible explanation for its evolutionary loss
dc.typeJournal article
pubs.publication-statusPublished

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